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The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits.

Oviedo HV, Bureau I, Svoboda K, Zador AM - Nat. Neurosci. (2010)

Bottom Line: By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column.In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3.Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

ABSTRACT
The primary auditory cortex (A1) is organized tonotopically, with neurons sensitive to high and low frequencies arranged in a rostro-caudal gradient. We used laser scanning photostimulation in acute slices to study the organization of local excitatory connections onto layers 2 and 3 (L2/3) of the mouse A1. Consistent with the organization of other cortical regions, synaptic inputs along the isofrequency axis (orthogonal to the tonotopic axis) arose predominantly within a column. By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column. In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3. Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

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Along tonotopic but not isofrequency axis, inputs to L3 arise asymmetrically out –of-column(a–b): L5/6 input to L3, but not L2, arose out-of-column preferentially from putative high-frequency neurons in tonotopic slices. Top panels show the distribution of the horizontal distances between the soma and its hotspot (ds–h) of presynaptic input along the tonotopic (n = 39) and isofrequency (n = 22) axes for each L2 and L3 neuron. The square points show the mean (± s.e.m) of the L2 and L3 distributions. Bottom panels show columnar average of L5/6 input. Asterisks indicate columns where input to L2 was significantly different from L3. The insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangle). (c) Local L3 input to L3 arose preferentially from putative high-frequency neurons in tonotopic slices. Relative contribution of local input (within L3) arising from the anterior and posterior (putative higher and lower frequency, respectively) input sites of the L3 cells mapped in the tonotopic slice. The plots show the mean charge transfer along columns. Input arising from the higher frequency sites was greater than from lower frequency sites in the tonotopic slice (left), but not the isofrequency (right). Inputs arising from posterior and medial sites were reflected on the x-axis for display purposes. Insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangles to the left and right of L3 somata). Data are presented as mean ± s.e.m.
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Figure 4: Along tonotopic but not isofrequency axis, inputs to L3 arise asymmetrically out –of-column(a–b): L5/6 input to L3, but not L2, arose out-of-column preferentially from putative high-frequency neurons in tonotopic slices. Top panels show the distribution of the horizontal distances between the soma and its hotspot (ds–h) of presynaptic input along the tonotopic (n = 39) and isofrequency (n = 22) axes for each L2 and L3 neuron. The square points show the mean (± s.e.m) of the L2 and L3 distributions. Bottom panels show columnar average of L5/6 input. Asterisks indicate columns where input to L2 was significantly different from L3. The insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangle). (c) Local L3 input to L3 arose preferentially from putative high-frequency neurons in tonotopic slices. Relative contribution of local input (within L3) arising from the anterior and posterior (putative higher and lower frequency, respectively) input sites of the L3 cells mapped in the tonotopic slice. The plots show the mean charge transfer along columns. Input arising from the higher frequency sites was greater than from lower frequency sites in the tonotopic slice (left), but not the isofrequency (right). Inputs arising from posterior and medial sites were reflected on the x-axis for display purposes. Insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangles to the left and right of L3 somata). Data are presented as mean ± s.e.m.

Mentions: We characterized the asymmetry of input to L3 with several analyses. First, to quantify the horizontal shift on a cell-by-cell basis, we computed the horizontal distance between the soma of the recorded neuron and its deep L5 and L6 hotspot (ds–h, see Methods for details). This analysis revealed a clear horizontal shift in the input to L3 (but not L2) in tonotopic slices, but none along the isofrequency axis (Fig. 4a–b, top). Unlike L2 neurons which received mainly columnar input, L3 cells received horizontally shifted inputs from as far as 400 µm away from the soma (P << 0.01, n = 39, t-test). Second, we calculated the average input arising from deep L5 and L6 from the average population maps (Fig. 4a–b, bottom). Consistent with the previous analysis of hotspots, this analysis revealed that inputs from deep L5 and L6 to L3 were shifted anteriorly with respect to L2 in tonotopic (Fig. 4a, bottom) but not isofrequency (Fig. 4b, bottom) slices. Because there is an anterior-posterior map of frequency in the primary auditory cortex, our results suggest that the input to L3 arises from out-of-column neurons in L6 tuned to higher frequencies.


The functional asymmetry of auditory cortex is reflected in the organization of local cortical circuits.

Oviedo HV, Bureau I, Svoboda K, Zador AM - Nat. Neurosci. (2010)

Along tonotopic but not isofrequency axis, inputs to L3 arise asymmetrically out –of-column(a–b): L5/6 input to L3, but not L2, arose out-of-column preferentially from putative high-frequency neurons in tonotopic slices. Top panels show the distribution of the horizontal distances between the soma and its hotspot (ds–h) of presynaptic input along the tonotopic (n = 39) and isofrequency (n = 22) axes for each L2 and L3 neuron. The square points show the mean (± s.e.m) of the L2 and L3 distributions. Bottom panels show columnar average of L5/6 input. Asterisks indicate columns where input to L2 was significantly different from L3. The insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangle). (c) Local L3 input to L3 arose preferentially from putative high-frequency neurons in tonotopic slices. Relative contribution of local input (within L3) arising from the anterior and posterior (putative higher and lower frequency, respectively) input sites of the L3 cells mapped in the tonotopic slice. The plots show the mean charge transfer along columns. Input arising from the higher frequency sites was greater than from lower frequency sites in the tonotopic slice (left), but not the isofrequency (right). Inputs arising from posterior and medial sites were reflected on the x-axis for display purposes. Insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangles to the left and right of L3 somata). Data are presented as mean ± s.e.m.
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Figure 4: Along tonotopic but not isofrequency axis, inputs to L3 arise asymmetrically out –of-column(a–b): L5/6 input to L3, but not L2, arose out-of-column preferentially from putative high-frequency neurons in tonotopic slices. Top panels show the distribution of the horizontal distances between the soma and its hotspot (ds–h) of presynaptic input along the tonotopic (n = 39) and isofrequency (n = 22) axes for each L2 and L3 neuron. The square points show the mean (± s.e.m) of the L2 and L3 distributions. Bottom panels show columnar average of L5/6 input. Asterisks indicate columns where input to L2 was significantly different from L3. The insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangle). (c) Local L3 input to L3 arose preferentially from putative high-frequency neurons in tonotopic slices. Relative contribution of local input (within L3) arising from the anterior and posterior (putative higher and lower frequency, respectively) input sites of the L3 cells mapped in the tonotopic slice. The plots show the mean charge transfer along columns. Input arising from the higher frequency sites was greater than from lower frequency sites in the tonotopic slice (left), but not the isofrequency (right). Inputs arising from posterior and medial sites were reflected on the x-axis for display purposes. Insets show the uncaging grid and the relative position of the cortical area where inputs were averaged (dashed rectangles to the left and right of L3 somata). Data are presented as mean ± s.e.m.
Mentions: We characterized the asymmetry of input to L3 with several analyses. First, to quantify the horizontal shift on a cell-by-cell basis, we computed the horizontal distance between the soma of the recorded neuron and its deep L5 and L6 hotspot (ds–h, see Methods for details). This analysis revealed a clear horizontal shift in the input to L3 (but not L2) in tonotopic slices, but none along the isofrequency axis (Fig. 4a–b, top). Unlike L2 neurons which received mainly columnar input, L3 cells received horizontally shifted inputs from as far as 400 µm away from the soma (P << 0.01, n = 39, t-test). Second, we calculated the average input arising from deep L5 and L6 from the average population maps (Fig. 4a–b, bottom). Consistent with the previous analysis of hotspots, this analysis revealed that inputs from deep L5 and L6 to L3 were shifted anteriorly with respect to L2 in tonotopic (Fig. 4a, bottom) but not isofrequency (Fig. 4b, bottom) slices. Because there is an anterior-posterior map of frequency in the primary auditory cortex, our results suggest that the input to L3 arises from out-of-column neurons in L6 tuned to higher frequencies.

Bottom Line: By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column.In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3.Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

View Article: PubMed Central - PubMed

Affiliation: Cold Spring Harbor Laboratory, Cold Spring Harbor, New York, USA.

ABSTRACT
The primary auditory cortex (A1) is organized tonotopically, with neurons sensitive to high and low frequencies arranged in a rostro-caudal gradient. We used laser scanning photostimulation in acute slices to study the organization of local excitatory connections onto layers 2 and 3 (L2/3) of the mouse A1. Consistent with the organization of other cortical regions, synaptic inputs along the isofrequency axis (orthogonal to the tonotopic axis) arose predominantly within a column. By contrast, we found that local connections along the tonotopic axis differed from those along the isofrequency axis: some input pathways to L3 (but not L2) arose predominantly out-of-column. In vivo cell-attached recordings revealed differences between the sound-responsiveness of neurons in L2 and L3. Our results are consistent with the hypothesis that auditory cortical microcircuitry is specialized to the one-dimensional representation of frequency in the auditory cortex.

Show MeSH
Related in: MedlinePlus